Rice pollen aperture formation is regulated by the interplay between OsINP1 and OsDAF1

Xu, Zhiwei; Zhao, Guochao; Tan, Qian; Yuan, Hui; Betts, Natalie S.; Zhu, Lu; Zhang, Dabing; Liang, Wanqi

doi:10.1038/s41477-020-0630-6

Cited by 41 publications

(86 citation statements)

References 34 publications

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“…The gene expression pattern of INP1 homologs during microsporogenesis also seems to be conserved across angiosperms. Similar to its counterparts in Arabidopsis and rice (Dobritsa and Coerper, 2012;Zhang et al, 2020), EcINP1 begins expression in pollen mother cells, reaches the maximum level at the early tetrad stage, and, after the release of microspores, its transcript practically disappears. In Arabidopsis, the AtINP1 protein signal disappears soon after the release of microspores from the tetrad, suggesting rapid degradation of the protein (Dobritsa and Coerper, 2012;Dobritsa et al, 2018).…”

Section: Discussionmentioning

confidence: 80%

“…Our pollen germination assay showed that apertures in E. californica, like those in Arabidopsis, are not essential for the exit of pollen tubes, and that pollen tubes can break through exine in inaperturate pollen grains. This is different from grasses, in which inaperturate mutants fail to germinate pollen tubes and show complete male sterility (Li et al, 2018;Zhang et al, 2020). Differences in exine morphology (thickness and tectum sculpture; Li et al, 2018) as well as in physiology of pollen and stigma (Edlund et al, 2016) have been proposed as possible causes for differences in dependence of pollen tubes on the presence of apertures.…”

Section: Discussionmentioning

confidence: 98%

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The Role of INAPERTURATE POLLEN1 as a Pollen Aperture Factor Is Conserved in the Basal Eudicot Eschscholzia californica (Papaveraceae)

et al. 2021

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Pollen grains show an enormous variety of aperture systems. What genes are involved in the aperture formation pathway and how conserved this pathway is in angiosperms remains largely unknown. INAPERTURATE POLLEN1 (INP1) encodes a protein of unknown function, essential for aperture formation in Arabidopsis, rice and maize. Yet, because INP1 sequences are quite divergent, it is unclear if their function is conserved across angiosperms. Here, we conducted a functional study of the INP1 ortholog from the basal eudicot Eschscholzia californica (EcINP1) using expression analyses, virus-induced gene silencing, pollen germination assay, and transcriptomics. We found that EcINP1 expression peaks at the tetrad stage of pollen development, consistent with its role in aperture formation, which occurs at that stage, and showed, via gene silencing, that the role of INP1 as an important aperture factor extends to basal eudicots. Using germination assays, we demonstrated that, in Eschscholzia, apertures are dispensable for pollen germination. Our comparative transcriptome analysis of wild-type and silenced plants identified over 900 differentially expressed genes, many of them potential candidates for the aperture pathway. Our study substantiates the importance of INP1 homologs for aperture formation across angiosperms and opens up new avenues for functional studies of other aperture candidate genes.

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Section: Discussionmentioning

confidence: 80%

Section: Discussionmentioning

confidence: 98%

The Role of INAPERTURATE POLLEN1 as a Pollen Aperture Factor Is Conserved in the Basal Eudicot Eschscholzia californica (Papaveraceae)

et al. 2021

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“…The DEFECTIVE IN APERTURE FORMATION1 (OsDAF1) is a lectin receptor-like kinase gene that is required for pollen aperture formation in which loss-of-function mutations cause poor annulus formation and male sterility. Moreover, mutations in OsDAF1 affects the colocalization of another gene, OsINP1, and results in the absence of the entire aperture and thus to no germination (Zhang X. et al, 2020).…”

Section: Pollen Germinationmentioning

confidence: 99%

Exploiting Genic Male Sterility in Rice: From Molecular Dissection to Breeding Applications

et al. 2021

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Rice (Oryza sativa L.) occupies a very salient and indispensable status among cereal crops, as its vast production is used to feed nearly half of the world’s population. Male sterile plants are the fundamental breeding materials needed for specific propagation in order to meet the elevated current food demands. The development of the rice varieties with desired traits has become the ultimate need of the time. Genic male sterility is a predominant system that is vastly deployed and exploited for crop improvement. Hence, the identification of new genetic elements and the cognizance of the underlying regulatory networks affecting male sterility in rice are crucial to harness heterosis and ensure global food security. Over the years, a variety of genomics studies have uncovered numerous mechanisms regulating male sterility in rice, which provided a deeper and wider understanding on the complex molecular basis of anther and pollen development. The recent advances in genomics and the emergence of multiple biotechnological methods have revolutionized the field of rice breeding. In this review, we have briefly documented the recent evolution, exploration, and exploitation of genic male sterility to the improvement of rice crop production. Furthermore, this review describes future perspectives with focus on state-of-the-art developments in the engineering of male sterility to overcome issues associated with male sterility-mediated rice breeding to address the current challenges. Finally, we provide our perspectives on diversified studies regarding the identification and characterization of genic male sterility genes, the development of new biotechnology-based male sterility systems, and their integrated applications for hybrid rice breeding.

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“…In other species, aperture positions, number, and morphologies can be different, suggesting the mechanisms guiding aperture formation are diverse. While the diversity of aperture patterns has captivated scientists for decades (Furness and Rudall, 2004;Matamoro-Vidal et al, 2016;Walker, 1974;Wodehouse, 1935), studies of the associated molecular mechanisms have only recently begun (Dobritsa and Coerper, 2012;Dobritsa et al, 2018;Lee et al, 2018;Reeder et al, 2016;Zhang et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

“…Aperture domains first become visible at the tetrad stage of pollen development, when four sister microspores, the products of meiosis, are held together under the common callose wall and aperture factors, such as INAPERTURATE POLLEN1 (INP1) and D6 PROTEIN KINASE-LIKE3 (D6PKL3) in Arabidopsis and OsINP1 and DEFECTIVE IN APERTURE FORMATION1 (OsDAF1) in rice, accumulate at distinct domains of the microspore plasma membranes (Dobritsa and Coerper, 2012;Dobritsa et al, 2018;Lee et al, 2018;Zhang et al, 2020). These domains become protected from exine deposition and develop into apertures (Dobritsa et al, 2018;Zhang et al, 2020). Yet how aperture domains are selected and what mechanism guides their patterning remains completely unknown.…”

Section: Introductionmentioning

confidence: 99%

Members of the ELMOD protein family specify formation of distinct aperture domains on the Arabidopsis pollen surface

Zhou

Amom

Reeder

et al. 2021

Preprint

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Pollen apertures, the characteristic gaps in pollen wall exine, have emerged as a model for studying the formation of distinct plasma-membrane domains. In each species, aperture number, position, and morphology are typically fixed; across species they vary widely. During pollen development certain plasma-membrane domains attract specific proteins and lipids and become protected from exine deposition, developing into apertures. However, how these aperture domains are selected is unknown. Here, we demonstrate that patterns of aperture domains in Arabidopsis are controlled by the members of the ancient ELMOD protein family, which, although important in animals, has not been studied in plants. We show that two members of this family, MACARON (MCR) and ELMOD_A, act upstream of the previously discovered aperture proteins and that their expression levels influence the number of aperture domains that form on the surface of developing pollen grains. We also show that a third ELMOD family member, ELMOD_E, can interfere with MCR and ELMOD_A activities, changing aperture morphology and producing new aperture patterns. Our findings reveal key players controlling early steps in aperture domain formation, identify residues important for their function, and open new avenues for investigating how diversity of aperture patterns in nature is achieved.

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Rice pollen aperture formation is regulated by the interplay between OsINP1 and OsDAF1

Cited by 41 publications

References 34 publications

The Role of INAPERTURATE POLLEN1 as a Pollen Aperture Factor Is Conserved in the Basal Eudicot Eschscholzia californica (Papaveraceae)

The Role of INAPERTURATE POLLEN1 as a Pollen Aperture Factor Is Conserved in the Basal Eudicot Eschscholzia californica (Papaveraceae)

Exploiting Genic Male Sterility in Rice: From Molecular Dissection to Breeding Applications

Members of the ELMOD protein family specify formation of distinct aperture domains on the Arabidopsis pollen surface

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